diversity

Review

Recent Advances in Understanding the Effects ofClimate Change on Coral Reefs

Andrew S. Hoey 1,*, Emily Howells 2, Jacob L. Johansen 3, Jean-Paul A. Hobbs 4,Vanessa Messmer 1, Dominique M. McCowan 1, Shaun K. Wilson 5,6 and Morgan S. Pratchett 1

1 ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville QLD 4811, Australia;vanessa.messmer@jcu.edu.au (V.M.); dominique.mccowan@my.jcu.edu.au (D.M.M.);morgan.pratchett@jcu.edu.au (M.S.P.)

2 Center for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi, UAE;em.howells@gmail.com

3 Department of Marine Science, University of Texas, Port Aransas, TX 78373-5015, USA;jacob.johansen@utexas.edu

4 Department of Environment and Agriculture, Curtin University, Bentley WA 6102, Australia;jp.hobbs@curtin.edu.au

5 Marine Science Program, Department of Parks and Wildlife, Kensington WA 6151, Australia;Shaun.Wilson@DPaW.wa.gov.au

6 Oceans Institute, University of Western Australia, Crawley WA 6069, Australia* Correspondence: andrew.hoey1@jcu.edu.au; Tel.: +61-7-4781-5979; Fax: +61-7-4781-6722

Academic Editor: Michael WinkReceived: 16 January 2016; Accepted: 11 May 2016; Published: 18 May 2016

Abstract: Climate change is one of the greatest threats to the persistence of coral reefs. Sustained andongoing increases in ocean temperatures and acidification are altering the structure and function ofreefs globally. Here, we summarise recent advances in our understanding of the effects of climatechange on scleractinian corals and reef fish. Although there is considerable among-species variabilityin responses to increasing temperature and seawater chemistry, changing temperature regimesare likely to have the greatest influence on the structure of coral and fish assemblages, at leastover short–medium timeframes. Recent evidence of increases in coral bleaching thresholds, localgenetic adaptation and inheritance of heat tolerance suggest that coral populations may have somecapacity to respond to warming, although the extent to which these changes can keep pace withchanging environmental conditions is unknown. For coral reef fishes, current evidence indicatesincreasing seawater temperature will be a major determinant of future assemblages, throughboth habitat degradation and direct effects on physiology and behaviour. The effects of climatechange are, however, being compounded by a range of anthropogenic disturbances, which mayundermine the capacity of coral reef organisms to acclimate and/or adapt to specific changes inenvironmental conditions.

Keywords: adaptation; acclimatization; thermal bleaching; ocean acidification; novel ecosystem;distorted food webs

1. Introduction

Climate change is having profound effects on the structure and functioning of ecosystemsworldwide, with increasing temperatures and changes in physiochemical characteristics leadingto shifts in taxonomic and functional composition, habitat degradation and loss, as well as declinesin biodiversity and productivity [1]. The effects of climate change are most pronounced in tropicalmarine ecosystems (e.g., coral reefs) [2,3], because many tropical marine species often have narrowthermal tolerances and live at or near their upper thermal limits (e.g., [4]). On coral reefs, the major

Diversity 2016, 8, 12; doi:10.3390/d8020012 www.mdpi.com/journal/diversity

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habitat forming organisms (scleractinian corals) operate so close to their upper thermal limit thatslight increases (ě1 ˝C) in temperature can cause large-scale mortality and habitat degradation [5].Although coral reefs have been exposed to changing climatic conditions repeatedly over geologicaltime [6,7], leading to the slowing or cessation of reef development, current environmental conditionsand rates of change appear to be beyond those experienced in the past [8].

Research into the effects of climate change on coral reefs was initially focused on the thermalsensitivities of corals (e.g., [5,9]) and the effects of acute broad-scale coral loss on reef-associatedorganisms [10,11]. More recently, there has been an increasing emphasis on: (i) understanding theindependent and interactive effects of ocean warming versus ocean acidification (oceanic uptake ofrising atmospheric CO2) [12]; (ii) the capacity of habitat-forming corals and reef-associated fishesto acclimatise and/or adapt to changing environmental conditions; and (iii) directional shifts in thestructure of reef communities and associated ecological feedbacks. The purpose of this review isto summarise recent advances in our understanding of the effects of climate change on coral reefs,focusing on taxa that have received the most attention in the literature; scleractinian corals andteleost fish.

2. Reef-Building Corals

2.1. Effects of Increasing Temperature

The most conspicuous effect of climate change on coral reefs thus far, has been so called“mass-bleaching” of scleractinian corals [3,13,14], which occurs when temperatures exceed thephysiological tolerances of a large number of different coral species. Thermal stress causes widespreaddeclines in the abundance of symbiotic zooxanthellae and their photosynthetic pigments, whichare the primary source of nutrition for most corals. While bleached corals can recover followingmoderate or short-term exposure to adverse environmental conditions, there have been some recentepisodes of extremely severe and widespread bleaching that resulted in extensive coral mortality(e.g., [14]), generating considerable concern about the fate of corals and coral reefs (e.g., [3,15]). In 1998,severe bleaching killed up to 90% of corals across much of the Indian Ocean, and environmentalconditions that caused this extensive coral loss are expected to recur almost annually within comingdecades [14,16,17]. Depending on the rate and magnitude of ongoing increases in ocean temperatures,coral-dominated habitats could become dominated by fleshy seaweeds, or at the very least, becomedrastically altered in terms of coral composition ([2,18], Table S1).

Projected climate change and associated increases in the incidence of mass coral bleaching haveled to dire predictions of wholesale coral loss, even as early as 2050 (e.g., [3,14]). However, bleachingsusceptibility varies greatly within and among coral taxa (e.g., [19,20]), suggesting there will be markedchanges in the structure of coral assemblages (e.g., [21]) rather than simultaneous and comprehensiveloss of scleractinian corals. There has been extensive research into bleaching susceptibility, mostlycomparing the proportion of colonies from different coral genera that bleach during a distinct bleachingevent. However, these data are almost universally based on studies at just one location (e.g., [9]) andthere have been very limited comparisons among locations (see [22]). A meta-analysis of data from68 different studies that document bleaching events in the Indo-Pacific (spanning Kenya to Panama),reveal the mean percentage of colonies that bleached ranges from 85.3% for Seriatopora down to<1.0% for Heliofungia (Figure 1). Given disproportionate effects on certain corals, ocean warmingand bleaching are likely to lead to shifts in coral composition (see also [23]). However, increasingincidence of coral bleaching will not necessarily favour those corals that have highest resistance toocean warming and bleaching [13,24]. Importantly, coral genera that exhibit highest rates of bleaching(e.g., Seriatopora, Stylophora, Acropora) are often capable of relatively rapid recovery in the aftermathof acute disturbances (e.g., [25]), owing to high rates of growth and recruitment. The extent towhich bleaching-resistant versus weedy corals come to dominate coral assemblages will depend on thefrequency versus severity of future mass-bleaching episodes (e.g., [26]). Frequent bleaching episodes are

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likely to suppress abundance of those corals that are the first and worst affected (e.g., Acropora, [22,27]),whereas infrequent but severe bleaching episodes will likely favor those corals that can recover rapidlyin the aftermath of such disturbances [24,25].

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[26]). Frequent bleaching episodes are likely to suppress abundance of those corals that are the first and worst affected (e.g., Acropora, [22,27]), whereas infrequent but severe bleaching episodes will likely favor those corals that can recover rapidly in the aftermath of such disturbances [24,25].

Figure 1. Taxonomic variation in bleaching susceptibility among 36 Indo-Pacific coral genera. Data presented is the percentage of coral colonies that exhibit bleaching, averaged across 68 studies conducted between 1982 and 2005, and spanning from Kenya to Panama (see [28] for specific details). Standard error bars indicate variation among 4–148 studies for each genus.

While extreme increases in ocean temperatures may cause extensive bleaching and mortality of corals (e.g., [13]), even moderate increases in temperature may have important demographic consequences for corals, moderating growth (e.g., [29]) and/or reproduction (e.g., [30]). The general relationship between an organism’s performance (e.g., growth and reproduction) and temperature is a hump-shaped curve, where moderate increases in temperature can have potentially beneficial effects on performance (Figure 2). However, exposure to ever increasing temperatures will ultimately lead to marked declines in organism performance (e.g., [29]), culminating in high levels of physiological stress (e.g., bleaching for corals) and mortality. On Australia’s Great Barrier Reef, there is recent evidence that growth rates of massive Porites have declined substantially since 1990 [31], which may be due to chronic increases in ocean temperatures and/or periodic cessation of growth following increasingly frequent and severe positive temperature anomalies and bleaching episodes [32]. Similarly, Cantin et al. [16] showed that growth rates of the robust coral, Diploastrea heliopora have declined by 30% since 1998 in the Red Sea (see also [33,34]). However, other studies (e.g., [35]) have revealed positive effects of increasing temperature on coral growth, mostly at high-latitude locations [36]. Declines in coral growth will impact directly on the resilience of corals to ongoing environmental change and disturbances, and also contribute greatly to sustained declines in cover of live corals [37].

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Figure 1. Taxonomic variation in bleaching susceptibility among 36 Indo-Pacific coral genera.Data presented is the percentage of coral colonies that exhibit bleaching, averaged across 68 studiesconducted between 1982 and 2005, and spanning from Kenya to Panama (see [28] for specific details).Standard error bars indicate variation among 4–148 studies for each genus.

While extreme increases in ocean temperatures may cause extensive bleaching and mortalityof corals (e.g., [13]), even moderate increases in temperature may have important demographicconsequences for corals, moderating growth (e.g., [29]) and/or reproduction (e.g., [30]). The generalrelationship between an organism’s performance (e.g., growth and reproduction) and temperature isa hump-shaped curve, where moderate increases in temperature can have potentially beneficial effectson performance (Figure 2). However, exposure to ever increasing temperatures will ultimately lead tomarked declines in organism performance (e.g., [29]), culminating in high levels of physiological stress(e.g., bleaching for corals) and mortality. On Australia’s Great Barrier Reef, there is recent evidence thatgrowth rates of massive Porites have declined substantially since 1990 [31], which may be due to chronicincreases in ocean temperatures and/or periodic cessation of growth following increasingly frequentand severe positive temperature anomalies and bleaching episodes [32]. Similarly, Cantin et al. [16]showed that growth rates of the robust coral, Diploastrea heliopora have declined by 30% since 1998in the Red Sea (see also [33,34]). However, other studies (e.g., [35]) have revealed positive effects ofincreasing temperature on coral growth, mostly at high-latitude locations [36]. Declines in coral growthwill impact directly on the resilience of corals to ongoing environmental change and disturbances, andalso contribute greatly to sustained declines in cover of live corals [37].

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Figure 2. Temperature performance curves for Pocillopora damicornis from Hawaii showing changes in calcification (open circles), following Jokiel and Coles [29] and standardised recruitment rates (grey circles), following Jokiel and Guinther [30] when corals are exposed to increasing temperature within experimental settings. Both growth and reproduction were optimal at ~26 °C, which corresponds with the normal summertime temperature to which these corals were naturally exposed [29].

2.2. Effects of Ocean Acidification

Coral reefs are reported to be among the most sensitive ecosystems to the ongoing effects of global climate change [38], not only because reef-building corals bleach, and often die, following even moderate increases in ocean temperatures, but because scleractinian corals are expected to be extremely sensitive to sustained and ongoing changes in seawater chemistry [3]. Changes in seawater chemistry (specifically, declines in pH and reduced availability of carbonate ions) are directly attributable to increases in atmospheric CO2 concentrations, and corresponding increases in the amount of anthropogenic CO2 dissolved in the oceans [39]. Experimental studies generally show that projected changes in seawater chemistry will compromise calcification rates of reef-building corals (e.g., [6,40–42]), but it is clear that effects of ocean acidification, like ocean warming, will vary both spatially and taxonomically. Notably, the locations that are least affected by ocean warming (e.g., high-latitude reefs) are likely to be the first and worst affected by declining aragonite saturation [36]. Ocean acidification also appears to exacerbate sensitivity of corals to increasing temperatures [43], resulting in higher severity of bleaching for a given increase in temperature. In microcosm experiments, Dove et al. [44] showed that many corals (Acropora, Seriatopora, Montipora and Stylophora) could not withstand the combination of elevated temperature and reduced aragonite saturation expected to occur on reefs by 2050, while some corals (e.g., Goniopora) did survive even though they bleached during warmer months.

Considerable research is still required to establish which corals will be “winners” and “losers” under changing climatic conditions (e.g., [45]) especially when it comes to considering the simultaneous effects of ocean warming and acidification. There is currently very limited data with which to assess which corals are more or less resilient to ocean acidification (but see [44]), though it does seem that changing temperature regimes (cf. changes in seawater chemistry) are going to have the greatest influence on the structure of local coral assemblages, at least in the short to medium term. Notably, there is increasing evidence that corals can effectively and efficiently regulate their internal pH [46] and thereby, mitigate the effects of ocean acidification [47]. Increasing physiological costs of pH regulation may lead to further declines in coral growth and reproduction [3], though the energetic impost may be minimal [46].

2.3. Acclimatisation and Adaptation of Reef-Building Corals

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Figure 2. Temperature performance curves for Pocillopora damicornis from Hawaii showing changes incalcification (open circles), following Jokiel and Coles [29] and standardised recruitment rates (greycircles), following Jokiel and Guinther [30] when corals are exposed to increasing temperature withinexperimental settings. Both growth and reproduction were optimal at ~26 ˝C, which corresponds withthe normal summertime temperature to which these corals were naturally exposed [29].

2.2. Effects of Ocean Acidification

Coral reefs are reported to be among the most sensitive ecosystems to the ongoing effects ofglobal climate change [38], not only because reef-building corals bleach, and often die, followingeven moderate increases in ocean temperatures, but because scleractinian corals are expected tobe extremely sensitive to sustained and ongoing changes in seawater chemistry [3]. Changes inseawater chemistry (specifically, declines in pH and reduced availability of carbonate ions) are directlyattributable to increases in atmospheric CO2 concentrations, and corresponding increases in theamount of anthropogenic CO2 dissolved in the oceans [39]. Experimental studies generally show thatprojected changes in seawater chemistry will compromise calcification rates of reef-building corals(e.g., [6,40–42]), but it is clear that effects of ocean acidification, like ocean warming, will vary bothspatially and taxonomically. Notably, the locations that are least affected by ocean warming (e.g.,high-latitude reefs) are likely to be the first and worst affected by declining aragonite saturation [36].Ocean acidification also appears to exacerbate sensitivity of corals to increasing temperatures [43],resulting in higher severity of bleaching for a given increase in temperature. In microcosm experiments,Dove et al. [44] showed that many corals (Acropora, Seriatopora, Montipora and Stylophora) could notwithstand the combination of elevated temperature and reduced aragonite saturation expected tooccur on reefs by 2050, while some corals (e.g., Goniopora) did survive even though they bleachedduring warmer months.

Considerable research is still required to establish which corals will be “winners” and “losers”under changing climatic conditions (e.g., [45]) especially when it comes to considering the simultaneouseffects of ocean warming and acidification. There is currently very limited data with which toassess which corals are more or less resilient to ocean acidification (but see [44]), though it doesseem that changing temperature regimes (cf. changes in seawater chemistry) are going to have thegreatest influence on the structure of local coral assemblages, at least in the short to medium term.Notably, there is increasing evidence that corals can effectively and efficiently regulate their internalpH [46] and thereby, mitigate the effects of ocean acidification [47]. Increasing physiological costs ofpH regulation may lead to further declines in coral growth and reproduction [3], though the energeticimpost may be minimal [46].

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2.3. Acclimatisation and Adaptation of Reef-Building Corals

Direct negative effects of climate change will continue to be experienced by corals in the nearfuture. However, available evidence indicates that at least some species and populations have thecapacity to acclimatise and/or adapt to warmer and more acidic conditions (Table S1f). Several coralspecies already persist in environments with similar conditions to those expected at the end of thecentury. Corals withstand 34–35 ˝C summers in the Persian Gulf, exhibiting bleaching thresholdsthat are ě2 ˝C higher than coral reefs elsewhere in the world [48]. Additionally, recent studiesshow that corals maintain calcification rates under low aragonite saturation states (Ωar < 1.0–2.5)at naturally acidified locations in the Indo-Pacific and Caribbean [49–51]. Notably, only a hardysubset of regional diversity is typically represented at these sites ([49,50,52] but see [53]) indicatingthat the scope to withstand future climate conditions is inherently variable among species andpopulations [20,44]. A caveat of this interpretation is the potential mismatch between historicaland contemporary rates of environmental change and evolution [54]. However, repeated thermalstress events over the past two decades provide new evidence that coral bleaching thresholds canincrease over relatively short timescales. Some of the genera that suffered the most severe bleaching inthe 1990s, including Acropora, Montipora, Stylophora and Pocillopora have exhibited increased resistanceto bleaching in the 2000s on the Great Barrier Reef [55,56], Southeast Asia [57], Moorea [58], andthe Maldives [59]. Follow-up species-specific investigations are required to determine whetherthese increases in bleaching resistance are due to acclimatisation of corals that recovered frominitial bleaching [60], selection for heat-resistant genotypes/epigenotypes (i.e., adaptation) [61], ora combination of these processes.

Interactions between multiple symbiotic partners shape the health, tolerance limits, andphenotypic plasticity of the coral holobiont [62,63]. The scope for the coral host and their complementof Symbiodinium to respond to environmental change is outlined herein, although other microbialpartners may also be important for coral evolution [64]. Coral hosts contribute to the stress toleranceof the symbiosis through the regulation of photoprotective and antioxidant systems [64,65], increasedheterotrophy [66], and potentially also symbiont cell densities [67]. Corals living in exceptionally warmlocations have been recently shown to exhibit higher levels of expression of candidate genes involvedin stress resistance traits compared with conspecifics in cooler environments [68–71]. For example,Acropora hyacinthus colonies living in a fluctuating thermal environment show elevated baselineexpression of multiple genes including heat shock proteins and antioxidants, which likely enablesan efficient response to regular pulses of temperature rise [68]. A proportion of these expressionsignatures is inducible by experience of warming, yet a remainder show fixed differences betweenpopulations, indicative of local adaptation [71–74]. For instance, positive host-driven acclimatisation hasbeen observed over days to years of exposure to warming [60,71,73,74]. For instance, Ainsworth et al. [74]recently showed that subjecting corals to sub-bleaching temperatures stress before reaching criticalbleaching temperatures decreased host cell mortality and Symbiodinium loss in Acropora aspera.If bleaching thresholds remain unchanged, the authors predicted that such an acclimatory mechanismwould be lost with future warming. Ultimately, the extent of acclimatisation remains constrainedby the genotypes of symbiont partners [71,75]. In the coral host, evidence for local adaptation totemperature is further supported by genetic differences between conspecific corals living in warmversus cool habitats in the absence of dispersal barriers (e.g., neighbouring back reef pools) [76].Heat stress experiments on the offspring of several corals including species of Acropora, Goniastrea,Platygyra and Porites confirm that local and regional variation in heat tolerance is passed ontooffspring [69,77–80]. Inheritance has been primarily attributed to genetic effects, [69,77,81], howeverepigenetic and maternal processes (forms of transgenerational acclimatisation) are also likely toinfluence the phenotype of host offspring [82]. Despite the examples provided, demographics ofcoral host populations including declining effective population sizes and relatively long generationtimes (first sexual reproduction at ~4–8 years) [83,84] suggest that they may not be able to keep pacewith contemporary warming [17,85]. However, information is currently lacking on other features of

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adaptive capacity including standing heritable variation for heat tolerance (but see [77,81,85]) andthe prevalence of somatic mutations, interspecific hybrids, and epigenetic modifications as sources ofnovel variation under selection [61,86–88].

Corals can also achieve large gains in their thermal tolerance over short timescales by formingassociations with heat tolerant Symbiodinium. Types (or “species”) of Symbiodinium vary widely in theircapacity to prevent and repair photosynthetic damage, which is a major source of oxidative stress in thecoral host [89–93]. Several (but not all) corals are able to take advantage of this diversity at symbiosisestablishment, either through non-specific uptake of Symbiodinium from the environment duringearly life-history [94] or maternal provisioning of multiple Symbiodinium genotypes [95]. Acute orchronic changes in temperature can cause shifts in the relative abundance of Symbiodinium typeswithin the host [96–100]. Classic examples are the greater prevalence of heat tolerant Symbiodinium D1(S. trenchi) [101] in several bleaching resistant or warm-water symbioses around the world (e.g., [102–105]).However, heat tolerance has evolved across Symbiodinium lineages [90], and recent studies have shownthat members of C1 [106,107] and C3 (S. thermophilum) [80,108] also exhibit exceptional heat tolerancein particular hosts and regions. Further characterisation of novel Symbiodinium types (e.g., [100]) andtheir physiology is expected to identify additional stress tolerant combinations. For Symbiodiniumtypes to continue to maintain functional mutualisms with their coral hosts, they will themselves needto adapt to warming. Traits of Symbiodinium populations including their large size (>108 per adulthost), fast asexual turnover (days to weeks), and cryptic sexual recombination are expected to maintainand generate high numbers of mutations upon which selection can potentially act [88,109–111], andresearchers are currently working towards quantifying adaptation rates in these important symbionts.

In comparison to temperature, relatively little is known about potential mechanisms involvedin maintaining net calcification under reduced aragonite saturation arising from increases in pCO2.Inter-species variation in physiological performance under elevated pCO2 generally favouring poritidsover acroporids and pocilloporids (e.g., [42,112–114]) has been linked to differential capacity toacclimatise via internal regulation of pH at the site of calcification [46]. Additionally, single specieshave been shown to be able to acclimatise to changes in pCO2 over days to weeks by recovering theirrespiration rate (Pocillopora damicornis) [82] or stabilising the expression of candidate genes involvedin metabolism and skeletal deposition (Acropora millepora) [115]. As with temperature, there is somecapacity to mediate energetic effects of acidification through increased heterotrophy [116], but there isno evidence (from limited data) to suggest that corals will associate with novel Symbiodinium partnersthat differ in performance under elevated pCO2 [117,118]. While initial research has investigatedtransgenerational acclimatisation to combined acidification and temperature stress [82], further workis required to disentangle positive and negative effects on offspring. At present, virtually no studieshave explored intra-species and -population variation in tolerance to elevated pCO2 (but see [42]) andwhether such variation has a heritable genetic basis (e.g., [119]). Yet, this information is critical inadvancing understanding of the potential of pCO2 sensitive species to persist under future acidification.

3. Reef Fishes

3.1. Direct Effects

While reef fishes will be widely affected by climate-induced changes in habitat composition andstructure (discussed below), ocean warming and acidification will also have substantive direct effects onphysiology, behaviour, abundance, distribution, and composition of reef fishes. Being ectotherms, themetabolic rates and energy requirement of reef fish are largely dictated by local water temperature [4,120],such that increasing temperatures will increase the rate of biochemical and cellular processes, andhence the energetic cost of activity, growth and reproduction [120]. Similarly, ocean acidification ispredicted to be energetically costly for reef fishes because they depend on a tightly regulated plasmapCO2 to facilitate oxygen binding and transport to tissues and organs. They regulate their internal

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acid-base balance, primarily through the differential excretion of H+ and HCO3- ions which becomes

increasingly more difficult against an acidic gradient [121].The energetic cost imposed by exposing fishes to increased temperatures is most apparent

by quantifying changes in metabolic rate and aerobic scope [4]. Numerous studies have reported30%–40% increases in basal metabolic energy requirements and substantive reductions in aerobicscope of coral reef fishes at temperatures 2–3 ˝C above current summer maxima (e.g., [122–126],Table S2), which is necessary for demanding physiological activities. Concurrent increases in energeticrequirements and reduced physiological capacity, suggest that any increases in temperature arelikely to negatively impact these species. Although energy requirements increase quickly with risingtemperatures (e.g., [127,128]), the direct implications of reduced aerobic scope on a species fitnessand ecology are unclear [129] largely because fishes can differentially allocate energy to growth,reproduction or activity. Notwithstanding these uncertainties, aerobic scope has been related toswimming performance [125], hypoxia tolerance [130] and competitive dominance [131] in some coralreef fishes. Johansen and Jones [125] showed that following a 3 ˝C increase in water temperatureseveral species of damselfish were no longer able to swim against the currents commonly encounteredin their respective coral reef habitats. Similarly, reductions in hypoxia tolerance under elevatedtemperatures could force some species to abandon shelters where oxygen levels frequently get depletedat night, such as within the branches of coral colonies, and move to more open habitats with greaterrisk of predation [130] or even relocate to cooler more oxygen rich waters [132,133].

A temperature-induced 30%–40% rise in energy demands and/or oxygen consumption is likelyto have direct implications for the viability of populations as available energy is directed away fromgrowth and reproduction and toward basal metabolic maintenance. Although enhanced larval growthand settlement success has been linked to small temperature increases within the natural range(e.g., [134,135]), recent experimental studies have shown that 1–3 ˝C increases in water temperatureled to marked reductions in somatic growth of both larval and adult coral reef fishes [136,137].These declines in growth were evident even when food supplies were increased [136,137] suggestingthere is limited capacity to compensate for the increased energy demands through elevated food intake.Similar results have been found in the large predatory reef fish, Plectropomus leopardus, with significantreductions in activity, movement and growth under 3 ˝C temperature increases even when providedwith unlimited food [128,138]. Such reductions in growth are likely to lead to increased larval durationand mortality rates, and reduced adult body size and productivity of reef fish populations underwarming oceans [139,140], particularly in large reef fishes which are likely to be more sensitive to theexpected temperature changes [141].

Available evidence also suggests that warming ocean temperatures will influence the reproductivebehaviour of coral reef fishes. Water temperature is an important trigger for production of reproductivehormones, gonad development and spawning [142,143]. Elevated ocean temperatures, therefore,may be expected to lead to earlier onset and shorter breeding season/s in the tropics compared tolonger breeding seasons at higher latitudes [144]. This potential effect on reproductive output isfurther offset by increased metabolic costs and reduced capacity for sustaining activity at elevatedtemperatures. Increases in water temperatures of 1.5–3.0 ˝C above current summer average on theGreat Barrier Reef (28.5 ˝C) led to marked declines in egg, clutch, and offspring size in the spinychromis, Acanthochromis polyacanthus, causing reduced reproductive output [136,145]. Although foodavailability moderated the effects of increased temperature on the number of breeding pairs, fishes ona high ration diet still produced fewer and smaller eggs, and smaller offspring [136].

In contrast to temperature, the effects of elevated CO2 on the aerobic scope, growth andreproduction of coral reef fish are less certain. The energetic cost of acid-base regulation underelevated CO2 is expected to affect respiration, circulation and metabolism of some fishes at extremelevels of environmental CO2 (>10,000 µatm) [146]. Empirical evidence for the negative effects onmetabolic performance at CO2 concentrations predicted for the next century (up to 1000 µatm) are,however, variable. The aerobic scope and growth rate of reef fishes has been reported to decrease,

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increase, or not change in response to elevated CO2 (e.g., [122,147–149], Table S3). Further, elevatedCO2 stimulated breeding activity in an anemonefish, with the number of breeding pairs, clutches perpair, and eggs produced per clutch being greater in fishes held at high (1000 µatm) CO2 compared tothose at control (430 µatm) CO2 [148,150].

The greatest effect of elevated CO2 on reef fishes appears to be through altered behaviour andsensory impairment. The vast majority of research suggests that, in the absence of adaptation,near-future CO2 levels (ca. 1000 µatm) will have a dramatic effect on the sensory abilities of reeffishes [151]. Numerous studies have reported acute exposure (mean = 7.46 days, range 4–28 days)to elevated CO2 to disrupt olfactory systems of fishes, in particular their ability to detect and avoidpredators (e.g., [152–155]), detect reefs and locate suitable settlement sites [147,153,156], and hencethe replenishment of reef fish populations. Exposure to elevated CO2 has also been shown to impairauditory [157] and visual systems [158], as well as general cognitive functions such as lateralisation,boldness, escape response, and learning [131,154,159,160]. Collectively, these effects have been shownto translate to a 5- to 9-fold increase in mortality for recently-settled damselfish exposed to elevatedCO2 and then released onto a reef [153,155]. Such an increase is critical given the already extremelyhigh mortality of fishes immediately following settlement (e.g., [161,162]). The prevalence of disruptedfunction across multiple sensory systems suggests that elevated CO2 affects central neural processingrather than individual sensory systems in isolation, and has been related to interference with a majorneurotransmitter receptor, GABA-A [151,163].

3.2. Acclimation and Adaptation of Reef Fish

Short-term acute exposure to elevated temperatures and pCO2 have marked effects on the fitnessand performance of reef fishes, however the longer-term effects of climate change will depend uponthe capacity of fishes to acclimate or adapt to changing conditions. While individual fishes appearto have limited capacity to acclimate to elevated temperature over several months [130,136], there issome evidence for localized adaptation in some traits of wild populations as well as experimentaldata suggesting developmental and transgenerational acclimation. Some wild-caught equatorial fishspecies have shown increased hypoxia tolerance befitting the greater severity and frequency of hypoxiain warmer regions [164]. Donelson et al. [123,124] demonstrated that rearing A. polyacanthus fromhatching at elevated temperatures (+1.5–3.0 ˝C) reduced their resting metabolic rate, with aerobicscope seeming to be completely restored to control levels when both parents and offspring were rearedunder these conditions. Thermally acclimated fish were, however, smaller and in poorer conditionthan control fish [123,124], and only fishes reared at 1.5 ˝C showed any capacity for reproductiveacclimation [145] suggesting physiological acclimation may come at a cost. Although this evidencefor physiological adaptation in this small-bodied species with short generation time is promising,the potential for other species with larger body size and longer generational times to acclimate toelevated temperature at the predicted rate of global warming is largely unknown. Given their increasedsensitivity many species may simply be forced to relocate to cooler regions with less severe hypoxicconditions [132] and less impact on reproductive capacity and timing [143,144].

The potential for fishes to acclimate to elevated CO2 is variable and appears to be largely traitdependent. Elevated CO2 reduced the growth and survival of juvenile anemonefish, however theseeffects were absent when the parents are also reared under elevated CO2 [148]. In contrast, declines inthe capacity of reef fishes to escape predators were not improved by transgenerational acclimation [160].Similarly, fishes in naturally acidic waters surrounding CO2 seeps in Papua New Guinea were foundto display similar behavioural abnormalities and sensory impairment as those reported in acuteexperimental studies [165]. Although this may be taken as evidence for limited scope of sensoryadaptation across generations it is likely confounded by the influx of individuals and genes fromunaffected areas around the seeps. Despite the behavioural abnormalities and sensory impairmentof the reef fishes tested from around the CO2 seeps there were limited differences in the richness,composition and abundance of fish assemblages between the seeps and adjacent control areas [165].

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Interestingly, several small prey fishes were more abundant around one of the seeps than control reefs,and it was hypothesized that this was related to differences in habitat between the seep and controlreefs. Similarly, the negative effects of elevated CO2 on the behavior and performance of temperatereef fish have been demonstrated to be dampened by habitat modification around CO2 seeps [166].

Until now, there has not been any research explicitly focused on the adaptive capacity of fishesto cope with climate-induced shifts in habitat availability, but anecdotal evidence suggests that anychanges in patterns of habitat-use, if apparent, are likely to negatively impact on affected populations.For highly specialised species, patterns of resource use appear insensitive to geographic variation inresource availability [167], suggesting that there will be limited capacity for temporal shifts in habitatuse. Even for species with flexible patterns of habitat use, preferred habitats often provide significantfitness advantages [168], and so populations that are restricted to suboptimal habitats are likely tohave slower growth, reduced fecundity, or even lower survivorship. Novel ecosystems that arisedue to fundamental shifts in habitat structure [169] are expected to support altogether different fishassemblages, dominated by habitat generalists or species with strong preferences for non-coral habitats.Influx of new species into established habitats have in the past resulted in strong dominance of singleinvasive species, similar to the lionfish explosion in the Caribbean [170], and similar scenarios mayalso unfold as tropical species start relocating into more subtropical and temperate regions [171,172].

3.3. Indirect Effects

Together with the effects on physiology and behaviour, climate induced changes to reef habitatsare already having a marked effect on the structure and function of reef fish assemblages [169,173,174].The increased frequency and/or severity of climate related disturbances, such as coral bleaching andstorms, are leading to declines in live coral cover, reductions in structural complexity, changes in coralcomposition and greater habitat fragmentation [12,175,176]. Indeed, ongoing degradation of coral reefhabitats is the most immediate pathway by which climate change will affect coral reef fishes [10,11].While <12% of reef fishes are considered to be directly reliant on live coral [177,178], a far greaterproportion of species (up to 75%, [179]) experience declines in abundance following extensive coralloss [169,180–184]. These declines likely reflect the reliance on live corals for food, refuge, settlementhabitat, or the greater availability of prey in coral rich areas [178,185].

Positive relationships between live coral cover and the abundance, biomass and/or diversity ofreef fishes are widespread (e.g., [179,180,186]). There is, however, substantial variation in the relianceon live corals among fish species, from dietary and habitat specialists that are highly dependent ona single coral species [187,188] to species that show no apparent association with live corals as eitherjuveniles or adults (e.g., [189]). Not surprisingly it is the obligate corallivores and habitat specialiststhat are the first to decline following widespread coral loss [10,11,190,191]. Reductions in the cover oflive coral are often accompanied by reductions in the topographic complexity of reef habitats due tothe dead coral skeletons being eroded by biological and physical forces [192–195]. It is this loss of thebiological and physical structure provided by scleractinian corals, however, that appears to have thegreatest impact on reef fish assemblages [196,197].

The structural complexity of reef habitats is a major determinant of reef fish abundance anddiversity (e.g., [184,196–199]), with this relationship typically associated to the role of corals increating complex three-dimensional habitats that increase habitat area and moderate biologicalinteractions. Importantly, live corals provide relatively fine-scale complexity, creating microhabitatsand refugia that mostly benefit small bodied and juvenile fishes [178,197,200]. As such, it has beenhypothesised that larger bodied fishes are less sensitive than smaller bodied fishes to coral loss(e.g., [201]). However, a recent meta-analysis of >400 coral reef fish species revealed no relationshipbetween fish body size and changes in abundance following coral loss, either with or without loss ofstructural complexity [173]. Although larger-bodied species with longer generation times may takelonger to respond, reductions in reef complexity will negatively affect both large- and small-bodiedfishes [184,202,203] and is predicted to reduce the productivity of coral reef fisheries [174,204,205].

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Together with reductions in coral cover and complexity, changes in the condition and compositionof coral assemblages are likely to have marked effects on reef fishes. Recently bleached corals (i.e., withskeletons intact) have been shown to support fewer species and individuals due to reduced settlementof some fish species [206,207], increased predation [208], and/or greater competition [209]. The effectof bleached corals is likely to be short-lived, with corals either recovering or dying within days toweeks. Subsequent changes in habitat configuration are, however, likely to have lasting effects on fishcommunities. The differential loss of some species under global warming and ocean acidification willalter coral diversity and community composition, and may lead to “novel” configurations [39,45,169].Many reef fish exhibit clear preferences for certain coral species (e.g., [178,210–212]) and highlyspecialised fish species are often disproportionately affected by coral depletion [213]. Different coralspecies and morphologies have been shown to support different fish assemblages (e.g., [199,214,215])thus the taxonomic and functional composition of reef fishes will depend on the composition offuture coral communities. In addition, the diversity of coral assemblages have been positively relatedto the species richness, and to a lesser extent the abundance, of fish assemblages in highly diversesystems [214,216]. Subsequently, reef fish assemblages in the most diverse systems may be themost vulnerable to changes in coral species composition and reductions in coral diversity, as thesecommunities tend to contain a greater proportion of habitat and dietary specialists [217]. While theeffects of reductions in fish species richness will be dependent on species identity, they are likely tonegatively affect the productivity and function of reef fish communities [218,219].

3.4. Ecological Feedbacks

Reductions in coral cover are often accompanied by increases in abundance of other alternativehabitat-forming organisms, such as macroalgae, that may further influence the behaviour, settlement,and survival of reef fishes. Indeed, a common response to loss of coral habitat is an increase inthe abundance and/or biomass herbivorous fish species (e.g., [9,220,221]). Increases in herbivorousfishes following coral decline is partially dependent on recruitment of juvenile fish and thereforehighly variable among species [11], and the increased availability of dietary sources. Increases inthe abundance of grazing parrotfishes and surgeonfishes following coral loss have been reported toreflect changes in the availability of the epilithic algal matrix (EAM sensu [222]) the preferred feedingsubstratum for these fishes.

Herbivorous fishes have been shown to avoid areas of high macroalgal density, presumably inresponse to elevated predation risk [223]. Recent experimental work has suggested that recently-settledreef fish (15 spp) use olfactory cues to avoid macroalgal-dominated habitats [224]. Such avoidanceis not, however, universal. Turf- and macro-algae that often dominate reefs following coral lossprovide habitat for many species of juvenile fish, including herbivorous species of parrotfish, rabbitfish,and surgeonfish [225–229] and increased abundance of these juvenile fishes contributes to uniqueassemblages of herbivores on macroalgal dominated reefs [230,231]. Some recent studies havesuggested grazing and browsing intensity on macroalgal-dominated reefs are broadly comparableto those on coral-dominated reefs [182,192,232], however there are few examples of herbivory beingsufficient to reverse macroalgal-dominance and promote the recovery of corals (see [218,233] forexceptions). If rates of herbivory are high, the extensive removal of fleshy macroalgae will promotecoral recovery, but will also lead to a loss of juvenile and adult habitat, and ultimately a decline in theabundance of herbivorous, and in particular browsing, fish [234]. Studies of recovering reefs in theSeychelles indicate that the capacity of browsing fishes to promote recovery is reliant on their biomassbeing >180 kg.ha [233], a value that is not commonly exceeded, even on relatively intact reefs withlimited fishing pressure [234,235].

A reduction in coral cover also places greater predation pressure on remaining corals byresident corallivores. Obligate coral feeding butterflyfish can remove up to 3 g of coral tissuea day [236], and selective feeding on certain coral species may account for 50%–80% of their annualproductivity [237]. On healthy reefs, where the cover of preferred corals is high, coral feeding by fish

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may be of little consequence. However, high susceptibility of corals preferred by many coral feeders(e.g., Acropora, Pocillopora) to environmental stress means their occurrence will decline followingdisturbances and remaining colonies will come under increased grazing pressure.

4. Conclusions

Coral reefs are considered among the most vulnerable ecosystems to sustained and ongoingchanges in environmental conditions due to climate change. Some corals do however, have exceptionalcapacity to withstand extreme temperatures, and fundamental shifts in environmental conditionsare likely to exert strong selective pressure on contemporary populations and communities. The keyissue however, is that coral reef ecosystems are being rapidly degraded not only due to climatechange, but also more direct anthropogenic disturbances, which may undermine the capacity of coralsand other reef-associated organisms to acclimate and/or adapt to specific changes in environmentalconditions [17,238]. For coral reef fishes, climate change will have important indirect effects (dueto coral loss and habitat degradation) as well direct effects on physiology, behaviour, abundance,distribution, and function. However, research has only just commenced to assess whether fishesmay acclimatise or adapt to these changing environmental conditions. Important components offuture research will be to test trans-generational acclimatisation and measure rates of contemporaryadaptation to synergistic changes in biotic and abiotic conditions across a broad range of taxa, as wellas the potential for species to behaviourally mitigate physiological limitations in performance.

Supplementary Materials: The following are available online at www.mdpi.com/1424-2818/8/2/12/s1, Table S1:Recently documented (last 5 years) effects of climate change on reef corals (a) declining coral cover; (b) reduceddiversity and shifts in coral community composition; (c) declining or low rates of coral calcification; (d) favourableconditions for higher latitude corals; (e) recent adaptation and/or acclimatisation (<20 years); and (f) longerterm adaptation and/or acclimatisation (unknown timescale); Table S2: Summary table of the effects of elevatedseawater temperature on the activity, development, metabolism, reproduction, and sensory capabilities of coralreefs fishes. “+” indicates positive, “-“ indicates negative, and “ns” no significant effect; Table S3: Summary tableof the effects of ocean acidification on the activity, development, metabolism, reproduction, sensory capabilities,and survival of coral reefs fishes. Numbers in parentheses for control and treatment CO2 are the pH of theseawater. “+” indicates positive, “-“ indicates negative, and “ns” no significant effect. ‘*’ denotes study wasconducted around natural CO2 seeps and as such an exposure time is not given.

Acknowledgments: We thank our partners and families for their ongoing and unconditional support of ourscientific pursuits, and to our many colleagues for useful discussions in preparing this review. Comments fromthe editor and three anonymous reviewers greatly improved the manuscript.

Author Contributions: Andrew S. Hoey and Morgan S. Pratchett conceived the idea and structure of the review;all authors contributed to the writing and editing of the review.

Conflicts of Interest: The authors declare no conflict of interest.

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